Influence of fish size in bioaccumulation of PCBs in seabass from semi-intensive aquaculture and natural environment
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1 Part 2 Influence of fish size in bioaccumulation of PCBs in seabass from semi-intensive aquaculture and natural environment Evidence for higher biomagnification factors of lower chlorinated PCBs in cultivated seabass Paulo Antunes, Odete Gil, Maria Armanda Reis-Henriques Science of the Total Environment 377 (2007) Combined effect of water and food contamination on PCB levels of seabass (Dicentrarchus labrax) in natural environment Paulo Antunes, Odete Gil, Maria Armanda Reis-Henriques Environmental Pollution, Submitted
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3 Influence of fish size in organochlorines bioaccumulation 49
4 Accumulation of PCBs and DDTs in Fish 50
5 Influence of fish size in organochlorines bioaccumulation 51
6 Accumulation of PCBs and DDTs in Fish 52
7 Influence of fish size in organochlorines bioaccumulation 53
8 Accumulation of PCBs and DDTs in Fish 54
9 Influence of fish size in organochlorines bioaccumulation 55
10 Accumulation of PCBs and DDTs in Fish 56
11 Influence of fish size in organochlorines bioaccumulation 57
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13 Influence of fish size in organochlorines bioaccumulation Combined effect of water and food contamination on PCB levels of seabass (Dicentrarchus labrax) in natural environment Paulo Antunes, Odete Gil, Maria Armanda Reis-Henriques Environmental Pollution, Submitted Abstract In the present work a bioaccumulation model was used to compare the relative importance of water and food as accumulation pathways. PCB concentrations in seabass tissues were related with water and food concentrations in natural environment of the coastal lagoon of Ria de Aveiro. Lipid normalized PCB concentrations had few differences between analyzed fish. Despite the similar total PCB concentrations, the lower chlorinated congeners showed accumulation patterns different than the higher chlorinated CBs. The model predicted a systematic overestimation of levels, suggesting that the measured dissolved concentration included some particles smaller than filter pore size. Dissolved concentrations were recalculated, based in suspended particulate matter (SPM) concentrations and the sediment water partition coefficient (K p ). The estimated concentrations ranged from 0.84 to 2.2 of the measured in Ria de Aveiro. The water had a higher contribution to accumulation for the lower chlorinated PCBs. Higher chlorinated PCBs accumulated almost exclusively from food. Keywords: PCB, Dicentrarchus labrax, Bioaccumulation model, Coastal lagoon INTRODUCTION The presence of polychlorinated biphenyls (PCBs) in the global ecosystem has been recognized since Risebrough et al. (1968), in particular in marine organisms (Jensen et al., 1969). In recent years there has been a great concern about the fish consumption risk for human health, in particular with farmed fish (Hites et al., 2004). The levels of PCBs in fish are reported in innumerable studies, including wild and farmed seabass in Portugal (Antunes et al., 2001; Antunes and Gil, 2004). The partitioning of PCB congeners among water, sediment and aquatic organisms are linked to the physicochemical properties of the compounds. Bioaccumulation of PCBs is also related to physiological and biochemical processes within the organisms. These processes are species dependent and animal size is recognised to influence the uptake, distribution and elimination of hydrophobic pollutants (Pastor et al., 1996). The sources of PCBs in fish are food and water (Moermond et al., 2004). The most common approach to evaluate bioaccumulation is to compare the levels in the organism with those in contamination sources (Kucklick et al., 1996). This comparison can be purely empirical, correlating measured concentrations with descriptors (such as K ow ), or mechanistic, which generally implement a mass balance approach in which the various transfer processes between compartments are quantified (Borga and Di Guardo, 2005). Between the variety of models that have been developed to simulate the bioconcentration of hydrophobic organic chemicals by fish, the allometric uptake models are those that allows us evaluate the different transfer processes and consider the biological determinants of uptake, mainly species and size specifics (Barber, 2003). In the present work a bioaccumulation model was used to compare the relative importance of water and food as accumulation pathways. PCB concentrations in seabass tissues were related with water and food concentrations in Ria de Aveiro, a coastal lagoon located in the northern of Portugal, permanently connected to the sea and that receives inputs from agriculture, urban and industrial activities. MATERIALS AND METHODS Sampling Seabass (Dicentrarchus labrax (Linnaeus, 1758)) were captured at Ria de Aveiro between August and November Length and weight were measured and fish grouped in three length classes (Table 1). Individuals were dissected and muscle and entrails content taken for chemical analysis. Muscle samples were 59
14 Accumulation of PCBs and DDTs in Fish prepared individually in samples from classes II and III, and in composite samples of 2-3 individuals for the smaller seabass. Two composite samples of entrails content were prepared for classes II and III. Sample tissues were freeze-dried. Water and SPM Fish is expected to move along the coastal lagoon so mean concentrations were considered to calculate bioaccumulation. Surface water was sampled in high- and low tide in September 1998 (during the sampling period of seabass) at seven stations of Ria de Aveiro. Samples were filtered through pre-washed (hexane) and pre-combusted (350 ºC, 17 h) Gelman A/E filters to separate dissolved and particulate fractions. The dissolved fraction was collected in glass flasks and analysed within two days. The filters were stored frozen until analysis. Table 1: Mean length (cm), weight (g) and standard deviation of the each size classes of seabass from Ria de Aveiro. Fish size class Number individuals of Length (cm) Weight I ± ± 3.9 II ± ± 15.3 III ± ± 24.4 (g) Materials The following materials were used for sample extraction and aliquot purification: n-hexane distilled in the laboratory, dichloromethane p.a. (Merck), sodium sulphate anhydrous (Merck), heated at 440 ºC overnight, Florisil mesh (Merck), activated at 440ºC overnight, and partially deactivated with 1% distilled water, and sulphuric acid p.a. (Merck). PCBs standard was obtained as a certified solution from AccuStandard Inc, (Q-CME-01). Analysis Analyses were performed as described in Antunes and Gil (2004). Fish tissues were Soxhlet extracted with n- hexane for 6 hours. SPM samples were Soxhlet extracted for 16 hours, and 2 L water were liquid-liquid extracted with n-hexane also. Fat content was determined gravimetrically from aliquots of tissue extracts. The remaining portion of the extracts was purified in a Florisil column and further with sulphuric acid. After concentration each sample was injected into a Hewlett Packard 5890 series II, equipped with a DB5 (J&W Scientific) capillary column (60 m, 0.25 mm I.D., 0.25 m film thickness) and an electron capture detector (ECD). A mixture of individual CBs was used as external standard for quantification. CBs 30, 65 and 204 were used as recovery standards. Detection limit, calculated as three times the standard deviation of blanks, ranged from 0.01 to 0.04 ng g -1. Statistical analysis One way analysis of variance or student s t-test was used to compare concentrations (Zar, 1996). A 5% significance level was used for all statistical tests. RESULTS AND DISCUSSION PCB congeners in water and SPM In Ria de Aveiro concentrations of PCB congeners were not significantly different (p<0.05) among sampling stations, and between high- and low tide, both in water and in suspended particulate matter (SPM). This suggests that spatial and temporal variations on PCB concentrations in water and suspended particles are poorly defined, in spite of the water volume exchanged between the Ria de Aveiro and the adjacent sea with the tide. Mean levels of PCBs in water and SPM recorded in Ria the Aveiro are presented in Table 2. The most abundant components in the dissolved fraction were the tri- to pentachlorinated congeners 18, 52, 44, 101 and 118, while CBs 18 (tri-), 118 (penta-), 153 and 138 (hexachlorobiphenyls) showed the highest concentrations in suspended particles. 60
15 Lipids and PCBs in seabass tissues Influence of fish size in organochlorines bioaccumulation The seventeen congeners quantified in this study were detected in almost all samples of muscle and entrails content. The average lipid content and CBs concentration (lipid normalized) for seabass are presented in Table 3. The fish s muscle presented low lipid content ( %) and juveniles (class I) presented lower lipid contents than bigger fish (class II and III). The dominant influence of lipid content on organochlorine compounds concentrations in aquatic biota is well established in the literature (Hebert and Keenleyside, 1995; Bentzen et al. 1996; Pastor et al., 1996). In this study, lipids explain 69% of the variability (given by the r 2 of the regression of tpcb versus lipids) in dry weight tpcb concentrations of the analysed fish in Ria de Aveiro. For this reason the CB concentrations were expressed in lipid basis. Table 2: Mean congener concentrations in water (ng L -1 ) and in suspended particulate matter (ng g -1 ) and standard deviation of samples collected in high and low tide in September 1998, in Ria de Aveiro, at fish sampling day (from Antunes et al., 2001). Congener Water (ng L -1 ) SPM (ng g -1 ) ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± < ± 0.06 The lipid basis concentrations of CBs in muscle, and entrails content of the three analyzed seabass classes are also presented in Table 3. Observing the total PCBs concentrations (calculated as the sum of the presented individual congeners) there were not found differences between size classes. Despite the similarity in total PCB concentrations, differences in congener s concentration in muscle among size classes were recorded. The smaller individuals showed higher concentrations of CBs with log K ow < 6.1. Smaller fish have higher contact with water so it is probable that they uptake a higher amount of these compounds from water than larger fish. Some differences were also observed in the penta- to heptachlorobiphenyls that presented higher contributions in individuals of class III. 61
16 Accumulation of PCBs and DDTs in Fish A Principal Component Analysis (PCA) of all results indicates that lipid content had the major influence in PCB accumulation, as seen before, and that the lower chlorinated CBs (18, 44, 49 and 52) had a different accumulation than all the others Figure 1. Table 3: Mean concentration (ng g -1 lip) of PCB congeners (± standard error) in muscle and in the entrails content of seabass from Ria de Aveiro. Muscle Entrails content I II III I II III Lipids (%) 2.6 ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± CB ± ± ± Total PCB ± ± ± Projection of the variables on the factor-plane ( 1 x 2) Factor 2 : 17.82% Remaining CBs Lipids Factor 1 : 71.32% Figure 1: PCA analysis of all the analysed samples. 62
17 Model application Influence of fish size in organochlorines bioaccumulation To evaluate the relative importance of uptake routes, a simple model using first order processes to describe PCB uptake in fish was applied based on equations provided by Thomann et al., 1992 and Hendriks et al., Uptake processes are: (1) absorption from water and (2) assimilation from food. Loss processes are excretion into water, egestion through food and internal processes like growth dilution. Metabolic transformation was assumed negligible for PCBs (Gobas, 1992). PCB uptake by fish can then be estimated using: dc dt fish = k ) C (1) abs, inc w + k ass1, inc food ( k excr, out + k eges, out + k grdil, out with C w the dissolved PCB concentration in water (ng g -1 ), C fish the PCB concentration in fish (ng g -1 wet wt) and C food the PCB concentration in food (ng g -1 wet wt). Rate constants k abs,in (absorption rate constant from water; (ng g -1 wet wt)/( ng g -1.d -1 )), k ass1,in (assimilation rate from food; (ng g -1 wet wt)/( ng g -1 wet wt.d -1 )), k excr,out (excretion rate into water; (d -1 )), k eges,out (egestion rate with food, (d -1 )) and k grdil,out (growth dilution rate constant, (d -1 )) are dependent on K OW and species weight and are estimated independently using allometric relationships (Hendriks et al. 2001, see supporting information). Other measured input values to the model were fish weight, fish and food lipid contents, PCB concentrations in fish and food, and water concentrations (Tables 1, 2 and 3). Log K ow values were taken from Hawker and Connell, Results were modelled from the smaller size, until the two other size classes. Figure 2 compares the estimated concentrations with the measured concentrations. The estimated concentrations are higher than the measured ones, within a factor of 3.3 to 53 for class II, and 2.5 to 37 for class III. These model results have deviations not higher than several other works (Borga and Di Guardo, 2005; Veltman et al., 2005), being the deviations generally explained by biological factors. However the fact that the model always overestimated the concentrations indicates a systematic error. These results also indicated a contribution of water contamination higher than the contribution of food. fish estimated [CB] (ng g -1. lip) Class II Class III x=y measured [CB] (ng g -1. lip) Figure 2: Estimated concentration of congeners vs. the measured concentrations in muscle (ng g -1 lip). Estimation based in measured water concentrations and entrails content concentrations. Values obtained with model estimation initialized with class I levels. Corrected dissolved water concentrations The water concentrations are the most sensitive factor in the estimations of fish contamination, due to low levels of the compounds and we do not know if the compounds are really dissolved or in suspended matter smaller than filter mesh (1µm). The dissolved concentration in water (C w ) is expected to be in equilibrium with SPM according to Mackay, 2001: 63
18 Accumulation of PCBs and DDTs in Fish C SPM K p = (2) Cw and K P = K f (3) OW OC with K P the sediment-water partition coefficient (l/kg) and f OC the fraction organic carbon in the SPM (0.05 g/g, Monterroso et al., 2003). The recalculated estimations using water concentrations based on SPM and Kp (Figure 3) presented a very good estimation of concentrations. The estimated concentrations ranged from 0.8 to 2.1 for class II, and 0.8 to 2.2 for class III of the measured concentrations. The only exceptions are the lower chlorinated congeners in class III that still had estimated concentrations from 5 to 11 times higher than the measured. The new estimation of trichlorobiphenyl (CB18) did not change significantly, and the tetrachlorobiphenyls (CB44, 49 and 52) estimated concentrations did present estimated concentrations 3 to 7 times closer to the measured in fish muscle. These results indicate that the bioavailability of PCBs in water is important to the correct determination of bioconcentration. The laboratorial determination of PCBs in water expresses not only the dissolved fraction, but also some PCBs adsorbed in particles smaller than filter porous. These very small particles have a big superficial area therefore they may have a high concentration of PCBs. estimated [CB] (ng g -1. lip) Class II Class III x=y measured [CB] (ng g -1. lip) Figure 3: Recalculated model concentration of Congeners vs. the measured concentrations in muscle (ng g -1 lip). Estimation based in dissolved water concentrations calculated applying partition coefficients (K p ) to SPM concentrations and entrails content concentrations. Values obtained with model estimation initialized with class I levels. From the used model we can also calculate separately the total uptake from water, the total uptake from food, and the elimination from water, food and growth dilution. Figure 4 presents the comparison between the water contribution to accumulation (difference between total uptake and elimination from water), and the food contribution to accumulation (difference between total uptake and elimination from food). The positive values do not always correspond to an increase of compound concentrations in fish due to the growth dilution. In adults the values are higher, as reflect of a higher time of simulation; the relative influence of the two pathways did not have significant differences between the two classes. The water had a higher contribution to accumulation for the lower chlorinated PCBs (CB18, 44, 49 and 52), PCBs with more than seven chlorine atoms (CB 170, 180, 183, 187 and 194) accumulated almost exclusively from food. The other CBs had similar contributions from water and food in the wild seabass. CONCLUSIONS It was possible to estimate the accumulation of PCBs in seabass from Ria the Aveiro, based in the environmental and food levels. For determination of dissolved fraction in water, we obtained better results when calculating based in the SPM concentrations and a partition coefficient (Kp) than analysing filtered 64
19 Influence of fish size in organochlorines bioaccumulation water. The filtered water contains small particles with large surface area which increased significantly the determined concentrations. uptake-elimination (ng g -1 ) Class II Congener water food Figure 4: Comparison between the estimated accumulation ( = uptake elimination) of PCB congeners from water and food in class II and III seabass from Ria de Aveiro. Values obtained with model estimation initialized with class I levels. Seabass accumulated PCBs through both of the possible pathways, water and food. The relative importance of each pathway depends on the compound hydrophobicity, lower chlorinated CBs had higher contribution from water than food. As expected water contribution decreased with hydrophobicity and food contribution increases. ACKNOWLEDGEMENTS Paulo Antunes acknowledge the PhD fellowship from the Portuguese Foundation for Science and Technology. REFERENCES Antunes, P., Gil, O., Costa, O., Accumulation pathways of PCBs in sea bass from Ria de Aveiro, Portugal. Ecotoxicology and Environmental Restoration 4, Antunes, P., Gil, O., PCB and DDT contamination in cultivated and wild sea bass from Ria de Aveiro, Portugal. Chemosphere 54, Barber, G., A review and comparison of models for predicting dynamic chemical bioconcentration in fish. Environmental Toxicology and Chemistry 22, Bentzen, E.D., Lean, R.S., Taylor, W.D., Mackay, D., Role of food web structure on lipid and bioaccumulation of organic contaminats by lake trout (Salvelinus namaycush). Canadian Journal of Fishery and Aquatic Science 53, Borga, K., Di Guardo, A., 2005, Comparing measured and predicted PCB concentrations in Arctic seawater and marine biota. Science of the Total Environment 342, Gobas, F., Modelling the Accumulation and Toxic Impacts of Organic Chemicals in Aquatic food- Chains. In: Gobas, F., McCorquodale, J. A., (Eds.), Chemical dynamics in fresh water ecosystems. Lewis Publishers, Chelsea, MI, USA, pp
20 Accumulation of PCBs and DDTs in Fish Hawker, D.W., Connell, D.W., Octanol-water partition coefficients of polychlorinated biphenyl congeners. Environmental Science and Technology 22, Hebert, C.E., Keenleyside, K.A., To normalize or not to normalize? Fat is the question. Environmental Toxicology and Chemistry 14, Hendriks, A.J., Heikens, A., The power of size II: rate constants and equilibrium ratios for accumulation of inorganic substances. Environmental Toxicology and Chemistry 20, Hendriks, A.J., Van der Linde, A., Cornelissen, G., Sijm, D. T. H. M., The power of size I: rate constants and equilibrium ratios for accumulation of organic substances related to octanol water partition ratio and species weight. Environmental Toxicology and Chemistry 20, Hites, R., Foran, J., Carpenter, D., Hamilton, M., Knuth, B., Schwager, S., Global assessment of organic contaminants in farmed salmon. Science 303, Jensen, S., Johnels, A.G., Olsson, M., Otterlind, G., DDT and PCB in marine animals from Sweedish waters. Nature 224, Kucklick, J., Harvey, H.R., Ostrom, P., Ostrom, N., Baker, J., Organochlorine dynamics in the pelagic food web of lake Baikal. Environmental Toxicology and Chemistry 15, Mackay D., Multimedia environmental models: the fugacity approach, second ed. Lewis Publishers, Boca Raton, pp Moermond, C., Roozen, F., Zwolsman, J., Koelmans, A., Uptake of sediment-bound bioavailable polychlorobiphenyls by benthivorous carp (Cyprinus carpio). Environmental Science and Technology 38, Monterroso, P., Abreu, S.N., Pereira, E., Vale, C., Duarte, A.C., Estimation of Cu, Cd and Hg transported by plankton from a contaminated area (Ria de Aveiro). Acta Oecologica 24, S351 S357. Pastor, D., Boix. J., Fernández, V., Albaigés, J., Bioaccumulation of organochlorinated contaminants in three estuarine fish species (Mullus barbatus, Mugil cephalus and Dicentrarcus labrax). Marine Pollution Bulletin 32, Risebrough, R.W., Rieche, P., Peakall, D.B., Herman, S.G., Kirven, M.N., Polychlorinated biphenyls in the global ecosystem. Nature 220, Thomann, R.V., Connolly, J. P., Parkerton, T.F., An equilibrium model of organic chemical accumulation in aquatic food webs with sediment interaction. Environmental Toxicology and Chemistry 11, Veltman, K., Hendriks, J., Huijbregts, M., Leonards, P., van den Heuvel-Greve, M., Vethaak, D., Accumulation of organochlorines and brominated flame retardants in estuarine and marine food chains: Field measurements and model calculations. Marine Pollution Bulletin 50, Zar, J.H., Biostatistical analysis, third ed. Ed. Prince-Hall Int. Inc. London. 66
21 Influence of fish size in organochlorines bioaccumulation Supporting Information OMEGA equations and parameters (Hendriks et al., 2001, Hendriks and Heikens, 2001) Internal concentration OMEGA calculates the concentration in organism (Ci) at time t according to: dc dt i, x = k 0, x, in C 0, w + k 1, x, in C i 1 j = 3 j= 1 k j, x, out C i Rate constants for uptake and elimination are correlated to species weight by allometric regressions. Additionally, these constants are inversely proportional to resistances in water and lipid layers (ρ) and flow delays. Uptake The rate constant for absorption of neutral organic compounds from water k 0,x,in (µg kg -1 wet wt / µg L -1 d -1 ): k 0, x, in = ρ H 2O,0 κ w ρ + K CH 2 ow 1 + γ 0 Rate constant for ingestion of neutral organic compounds with food k 1,x,in k 1, x, in ƒ as = 1- ƒ as p CH 2, i 1 1 ( K ow 1) + 1 ρ H 2O, food ρch 2 + K q ow t: c + w κ p CH 2, i 1 K 1 ow ( 1 ƒ as ) γ 1 Elimination rate constants Total elimination rate, equals the sum of elimination via excretion, egestion and growth dilution: 2 k j, x, out = k0, xout + k1, xout + k2, x, out 0 1) Neutral organic compounds: Rate constant for excretion via water k o,x,out : k o, x, out = p CH 2, i 1 ( K 1) ow + 1 ρ H 2O,0 κ w ρ + K CH 2 ow 1 + γ 0 Rate constant for egestion with food k 1,x,out : k 1, x, out = p CH 2, i 1 ( K ) ow ρ H 2O, food Rate constant for dilution of biomass k 2,x,out : k = q γ w 2, x, out t: c 2 κ ρ + q K t: c CH 2 ow + p w κ CH 2, i 1 K ow 1 1 ( ƒ as ) qt: c γ 1 67
22 Accumulation of PCBs and DDTs in Fish Table S1: Factors used in equations with typical or default values for parameters (Hendriks et al., 2001, Hendriks & Heikens, 2001) Symbol Description Unit Typical value (measured values in bold) C i Concentration in organism kg kg -1 wet weight C 0,w Concentration in water kg L -1 C i-1,x Concentration in food kg kg -1 wet weight k o,x,in Substance absorption rate constant kg kg -1 wet wt d -1 / kg L -1 k 1,x,in Substance assimilation rate constant kg kg -1 d -1 / kg kg -1 - k o,x,out Substance excretion rate constant kg -1 /kg -1 d -1 = d -1 k 1,x,out Substance egestion rate constant kg -1 /kg -1 d -1 = d -1 k 2,x,out Substance dilution rate constant kg -1 /kg -1 d -1 = d -1 f as Fraction of ingested food assimilated 80% for fish species γ 0 Water absorption excretion coefficient kg κ d (water-breathing) γ 2 Biomass (re)production coefficient kg κ d γ 1 Food ingestion coeficient kg κ d κ Rate exponent / 0.25 p CH2,,i-1 Lipid fraction of food (i-1) kg lipid wt / kg wet wt 0.16 p CH2,i Lipid fraction of organism (i) kg lipid wt / kg wet wt ρ CH2 Lipid layer resistance for in /efflux of d kg -κ 68 organic substances in animals ρ H2O,0 Water layer resistance from / to water d kg -κ ρ H2O,food Water layer resistance from / to food d kg -κ q T:c Temperature correction factor kg kg -1 1 (cold-blooded), W Species weight kg 68
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